The known world
fauna of aphids (Aphidinea) recently reached a total of 5000 species, placed
in 510 currently accepted genera. About half of these species spend all or
part of their life feeding on trees, and it can be seen from Table 1
that all the major groups of aphids are mostly or even entirely associated
with trees. The proportion of tree-living aphid species is probably even
higher than indicated, as the unknown hosts of many species are likely to be
trees. The trees most favoured as hosts tend to be the older evolutionary
groups such as Coniferae, Lauraceae, Fagaceae, Betulaceae, Hamamelidaceae,
Ulmaceae and Juglandaceae, and it seems likely that the major groups of
aphids differentiated before the appearance of herbaceous plants. Only three
groups at or above the tribal level live only on herbs; the Saltusaphidinae
which live on Cyperaceae and Juncaceae, the Siphini (subfamily
Chaitophorinae) living on Gramineae/Poaceae, and the Tramini (subfamily
Lachninae) living mostly on roots of Compositae/Asteraceae.

Nevertheless, aphid species collectively have been
recorded from about 300 plant families (Table 2),
including many of the more recent families of mainly herbaceous flowering
plants. Some of these families (marked by an asterisk in Table 2) only have
the most polyphagous aphid species recorded from them, but there are also
very numerous host plant-aphid associations at the genus or species level,
without which it would have been impossible to have compile the host-oriented
keys on this website. The discrepancy is mainly due, as can be seen by
comparing aphid species numbers in Table 1,
to the massive recent expansion of the largest subfamily Aphidinae. Many
members of both tribes within this subfamily (Aphidini and Macrosiphini)
retain an association with woody hosts, usually Rosaceae, but migrate for the
summer to a wide variety of herbaceous plants, including ferns and mosses as
well as angiosperms, and some of the largest genera of Macrosiphini live
exclusively on herbaceous plants. For a review of aphid-host plant associations
and how they may have evolved see Peccoud et
al. (2010).

Aphids are predominantly a northern temperate group,
with remarkably few species in the tropics. Dixon et al. (1987) postulated that the great diversity of the tropical
forest fauna mitigates against short-lived host-specific insects such as
aphids. Certainly the absence of aphids from many tropical forest trees is
striking, with whole families (e.g. Dipterocarpaceae) seemingly almost immune
from attack. The absence of records of aphids from economically important
tropical forest trees such as mahogany (Swietenia mahogoni, Meliaceae)
and rosewood (Dalbergia nigra, Leguminosae) can hardly be due to
negligence by collectors, and suggests that aphids really do not occur on
such trees, or at least do little damage. We think, however, that the
explanation for this can be found in the evolutionary history of aphids
rather than in their present-day host relations or ecology. Psyllids have
similar ecology and host relations to aphids, yet many tropical trees with
few aphids bear a large psyllid fauna. It seems likely to us that aphids have
failed to diversify in the tropics because of one particular, primitive
feature of aphid biology, their cyclical parthenogenesis.

Cyclical parthenogenesis is a very successful way of
exploiting the short-lived growth flushes of temperate plants, and aphids are
thus a very successful group in temperate climates, using seasonal clues to
time the alternation of the sexual and parthenogenetic phases of their life
cycles (see below). Such life cycles cannot however be readily adapted to
tropical conditions. Aphids moving from temperate zones into the tropics
simply lose the sexual phase of the life cycle, and in doing so they lose the
potential to evolve and diversify that is dependent on the recombination of
genes. The tropics may also have acted in this way as a barrier to aphid
colonization of southern temperate regions, which also have very small
indigenous aphid faunas.

The occurrence of Neophyllaphis on Podocarpus,
Araucaria and related conifers throughout the southern continents
testifies to the age of aphid-tree relationships, but very little is known
about such evolutionarily ancient associations. Most ecological and
experimental studies of aphid-tree interactions have concerned introduced
species. In Britain,
economic damage to spruce by sporadic outbreaks of Elatobium abietinum
has been documented since 1846. Damage to the more recently introduced Picea
sitchensis is particularly severe, heavy infestations resulting in complete
needle loss. Aphid infestations have been shown to reduce the accretion of
wood (e.g. of sycamore; Dixon,
1971a), and have deleterious effects on tree root growth (e.g. of Tilia;
Dixon,
1971b). However, none of these trees is native to Britain. There are no native
British Picea, sycamore is an
introduction from Central Europe, and the
common British lime tree (or linden) is thought to be a hybrid between a
native and an introduced species.

Planted forests of exotic trees cover enormous areas
of the globe. There are more than 5.5 million hectares of planted forests in Brazil, of
which at least 40 are Eucalyptus spp. (Anon., 1985). Pinus radiata
occupies only a small area in its native California but has been widely planted in New Zealand
and elsewhere. During this century many European, oriental and American
species of Pinus were introduced to various parts of Africa
and grew aphid-free for many years. In recent times three aphids, Eulachnus
rileyi from Europe, Cinara cronartii
from North America and Pineus boerneri
of uncertain origin, have appeared on pines in Africa
and caused far greater damage than they do in Europe
or America.
Similarly, Cinara cupressi is much more damaging to Cupressaceae in Africa than in Europe.
These exotic conifers may be growing under stress, and the aphids are
certainly without the complex of natural enemies associated with them in
their countries of origin.

Most aphid damage to trees seems to result directly
from feeding, either by removal of sap or wounding of tissue, or in at least
some cases by the toxic effect of saliva. Aphids are rarely recorded as
vectors of viruses infecting trees (Biddle and Tinsley, 1967). Given the
astronomical numbers of aphids in the air and the length of life of trees,
there must be strong selection among trees for resistance to
aphid-transmitted viruses. It would be interesting to know the mechanism of
this resistance, and whether it could be transferred to shorter-lived crop
plants. Perhaps the energy required to maintain such defences would be
uneconomic for annual or biennial plants.

The problem of how a long-lived plant genotype such
as an individual tree survives, when its herbivores have numerous generations
in which to evolve methods of breaking its defences, is discussed by Whitham
(1983), who showed that there is a similar range of resistance to attack by Pemphigus
betae among different branches of one cottonwood tree, as there is among
trees in a population. He concluded that long-lived plants are mosaics of
phenotypic and/or genetic variability, the genetic differences possibly
arising by somatic mutation (Whitham and Slobodchikoff, 1981).

Alstad and Edmunds (1983) found that the black
pine-leaf scale, Nuculaspis californica, seemed to establish demes
with genetic adaptations to counteract the defence patterns of individual
ponderosa pine trees. It is not known whether any aphids develop such
long-term natural associations. Tree-dwelling aphids, especially those of the
large subfamily Calaphidinae, tend to be rather more active insects than the
aphids which colonize herbaceous plants, and may frequently move between
trees - although the extent of movement by individual aphids is still largely
unknown. Most aphid species in several other subfamilies alternate annually
or biennially between their tree host and a herbaceous host (see below), and
therefore cannot develop genotype-specific associations, unless of course
they were to return to the same tree year after year.

Aphid life cycles
can be quite complicated and involve a succession of morphologically
different forms (morphs) of the same species. The complexity – and the
terminology created to describe it - can be daunting to the non-specialist.
Rather than add to the pages of descriptive text already available on aphid
life cycles (e.g. Hille Ris Lambers 1966d, Blackman 1974, Dixon 1985,
Miyazaki 1987), we will merely summarize the essential features, avoiding
jargon as much as possible, and use diagrams (Figs 1-7; links below) to
illustrate typical life cycles of tree-dwelling aphids. Some unavoidable
additional terminology - for example that needed to describe adelgid morphs
and life cycles - can be picked up by studying the life cycle diagrams. The
essential features of aphid life cycles are:

1. The various families
and subfamilies of Aphidoidea each have life cycles with characteristic
features, indicating that they have evolved independently.

2. A complete life
cycle (that is, a holocycle) typically consists of one generation of sexual morphs
(sexuales) and several generations in which only parthenogenetic females are
produced. This phenomenon of cyclical parthenogenesis is a basic, primitive
feature of aphid biology.

3. In the more
primitive families, Adelgidae and Phylloxeridae, both sexual and
parthenogenetic females are oviparous, but in the Aphididae parthenogenetic
females always give birth to live young; in Aphididae the parthenogenetic
females are therefore termed viviparae, and the sexual females are
distinguished as oviparae.

4. The more complex
life cycles involve host alternation; the technical term is heteroecy. In
heteroecious aphids, the sexuales mate and fertilized eggs are laid on a tree
or shrub, the primary host, but a regular migration occurs at some stage in
the life cycle to another, totally unrelated plant, which may be herbaceous
or woody - the secondary host. On the secondary host, only parthenogenetic
generations (exules) occur, and a return migration to the primary host is
needed before the next sexual generation.

5. Because host
alternation has evolved several times independently in Aphidoidea, there are
important differences at the family and subfamily levels in the way in which
it is achieved (see Figs 1-4, links below). It may occur as part of a
one-year cycle (this happens in all Aphidinae, most Hormaphidinae,
Pemphigini, Eriosomatini), or the complete cycle may take two years
(Adelgidae, Fig.
1; Fordini, Fig.
2). Some Hormaphidinae have now been shown to have long-lasting galls on
their primary hosts, that do not mature for 2-5 years.

6. The great
majority of aphids go through both the sexual and parthenogenetic phases of their
life cycle on one host plant, or on a small range of closely-related plants.
The technical term for this is monoecy. Calaphidinae, Drepanosiphinae,
Chaitophorinae, Greenideinae and Lachninae do not have host alternation; all
species in these subfamilies are monoecious. Some examples of monoecious life
cycles are depicted in Figs 5, 6 and 7 (links below). Monoecious aphids
generally have fewer morphs, and there are smaller differences between
morphs, than in heteroecious aphids, although there may be considerable
seasonal variation.

7. Some aphids have
lost the sexual part of the life cycle; that is, they are anholocyclic. Some
species are entirely anholocyclic and have no known sexual morphs (e.g. Tuberolachnus
salignus, Pineus boerneri,
Myzus ascalonicus), while others may be anholocyclic in warmer
climates and holocyclic in cold temperate regions (e.g. Eulachnus rileyi, Myzus persicae).
Populations of certain species maintain the options of both sexual and
parthenogenetic reproduction in mild climates, by producing sexuales while at
the same time continuing to produce parthenogenetic females (e.g. many
Greenideinae). Anholocyclic populations of heteroecious aphids lose their
link with the primary host and live all year reproducing parthenogenetically
on secondary host plants.